Cornichon-2 modulates AMPA receptor-transmembrane AMPA receptor regulatory protein assembly to dictate gating and pharmacology

Journal of Neuroscience

Volumn 31, Issue 18, 2011, Pages 6928-6938

  Gill, Martin B ^a   Kato, Akihiko S ^a   Roberts, Matthew F ^a   Yu, Hong ^a   Wang, He ^a   Tomita, Susumu ^b   Bredt, David S ^a  

^a ELI LILLY AND COMPANY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; BINDING PROTEIN; CORNICHON 2; REGULATOR PROTEIN; TRANSMEMBRANE AMPA RECEPTOR REGULATORY PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CEREBELLUM; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PURKINJE CELL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CEREBELLAR CORTEX; ELECTROPHYSIOLOGY; HIPPOCAMPUS; ION CHANNEL GATING; MALE; MEMBRANE PROTEINS; MICE; NEURONS; PROTEIN SUBUNITS; RATS; RATS, WISTAR; RECEPTORS, AMPA;

EID: 79955761295     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6271-10.2011     Document Type: Article

References (34)

1. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408:936-943.
2. Cho CH, St-Gelais F, Zhang W, Tomita S, Howe JR (2007) Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 55:890-904.
3. Collingridge GL, Olsen RW, Peters J, Spedding M (2009) A nomenclature for ligand-gated ion channels. Neuropharmacology 56:2-5.
4. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
5. Fukaya M, Yamazaki M, Sakimura K, Watanabe M (2005) Spatial diversity in gene expression for VDCCgamma subunit family in developing and adult mouse brains. Neurosci Res 53:376-383.
6. Fukaya M, Tsujita M, Yamazaki M, Kushiya E, Abe M, Akashi K, Natsume R, Kano M, Kamiya H, Watanabe M, Sakimura K (2006) Abundant distribution of TARP gamma-8 in synaptic and extrasynaptic surface of hip-pocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur J Neurosci 24:2177-2190.
7. Greger IH, Khatri L, Kong X, Ziff EB (2003) AMPA receptor tetrameriza-tion is mediated by Q/R editing. Neuron 40:763-774.
8. Hashimoto K, Fukaya M, Qiao X, Sakimura K, Watanabe M, Kano M (1999) Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J Neurosci 19:6027-6036.
9. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
10. Kato AS, Zhou W, Milstein AD, Knierman MD, Siuda ER, Dotzlaf JE, Yu H, Hale JE, Nisenbaum ES, Nicoll RA, Bredt DS (2007) New transmembrane AMPA receptor regulatory protein isoform, γ-7, differentially regulates AMPA receptors. J Neurosci 27:4969-4977.
11. Kato AS, Siuda ER, Nisenbaum ES, Bredt DS (2008) AMPA receptor subunit-specific regulation by a distinct family of type II TARPs. Neuron 59:986-996.
12. Kato AS, Gill MB, Ho MT, Yu H, Tu Y, Siuda ER, Wang H, Qian YW, Nisenbaum ES, Tomita S, Bredt DS (2010) Hippocampal AMPA receptor gating controlled by both TARP and cornichon proteins. Neuron 68:1082-1096.
13. Kim KS, Yan D, Tomita S (2010) Assembly and stoichiometry of the AMPA receptor and transmembrane AMPA receptor regulatory protein complex. J Neurosci 30:1064-1072.
14. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176.
15. Mansour M, Nagarajan N, Nehring RB, Clements JD, Rosenmund C (2001)Heteromeric AMPA receptors assemble with a preferred subunit stoichi-ometry and spatial arrangement. Neuron 32:841-853.
16. Mayer ML, Armstrong N (2004) Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66:161-181.
17. Menuz K, &/x&&namegr type=editor&&name&&sname&Nicoll&/sname&&x& &/x&&fname&RA&/fname&&/name&&/namegr& (2008) Loss ofinhibitory neuron AMPA receptors contributes to ataxia and epilepsy in stargazer mice. J Neurosci 28:10599-10603.
18. Milstein AD, Zhou W, Karimzadegan S, Bredt DS, Nicoll RA (2007) TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55:905-918.
19. Morimoto-Tomita M, Zhang W, Straub C, Cho CH, Kim KS, Howe JR, Tomita S (2009) Autoinactivation of neuronal AMPA receptors via glutamate-regulated TARP interaction. Neuron 61:101-112.
20. Moss FJ, Dolphin AC, Clare JJ (2003) Human neuronal stargazin-like proteins, gamma2, gamma3 and gamma4; an investigation of their specific localization in human brain and their influence on CaV2.1 voltage-dependent calcium channels expressed in Xenopus oocytes. BMC Neuro-sci 4:23.
21. Patneau DK, Vyklicky L, Mayer ML (1993) Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J Neu-rosci 13:3496-3509.
22. Rouach N, Byrd K, Petralia RS, Elias GM, Adesnik H, Tomita S, Karimzade-gan S, Kealey C, Bredt DS, Nicoll RA (2005) TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nat Neurosci 8:1525-1533.
23. Schwenk J, Harmel N, Zolles G, Bildl W, Kulik A, Heimrich B, Chisaka O, Jonas P, Schulte U, Fakler B, Klocker N (2009) Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323:1313-1319.
24. Seeburg PH (1993) The TINS/TiPS Lecture. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:359-365.
25. Shi Y, Lu W, Milstein AD, Nicoll RA (2009) The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62:633-640.
26. Shi Y, Suh YH, Milstein AD, Isozaki K, Schmid SM, Roche KW, Nicoll RA (2010) Functional comparisonofthe effectsofTARPs and cornichons on AMPA receptor trafficking and gating. Proc Natl Acad Sci U S A 107:16315-16319.
27. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462:745-756.
28. Soto D, Coombs ID, Renzi M, Zonouzi M, Farrant M, Cull-Candy SG (2009) Selective regulation of long-form calcium-permeable AMPA receptors by an atypical TARP, gamma-5. Nat Neurosci 12:277-285.
29. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, Bredt DS (2003) Functional studies and distribution define a family of transmem-brane AMPA receptor regulatory proteins. J Cell Biol 161:805-816.
30. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA, Bredt DS (2005) Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435:1052-1058.
31. Tomita S, Byrd RK, Rouach N, Bellone C, Venegas A, O'Brien JL, Kim KS, Olsen O, Nicoll RA, Bredt DS (2007) AMPA receptors and stargazin-like transmembrane AMPA receptor-regulatory proteins mediate hippocam-pal kainate neurotoxicity. Proc Natl Acad Sci USA 104:18784-18788.
32. Vandenberghe W, Nicoll RA, Bredt DS (2005) Stargazin is an AMPA receptor auxiliary subunit. Proc Natl Acad Sci USA 102:485-490.
33. Wang R, Walker CS, Brockie PJ, Francis MM, Mellem JE, Madsen DM, Mar-icq AV (2008) Evolutionary conserved role for TARPs in the gating of glutamate receptors and tuning of synaptic function. Neuron 59:997-1008.
34. Yamazaki M, Fukaya M, Hashimoto K, Yamasaki M, Tsujita M, Itakura M, Abe M, Natsume R, Takahashi M, Kano M, Sakimura K, Watanabe M (2010) TARPs gamma-2 and gamma-7 are essential for AMPA receptor expression in the cerebellum. Eur J Neurosci 31:2204-2220.